Emerging viral diseases of pollinating insects

Abstract

The risks posed by rapidly evolving RNA viruses to human and animal health are well recognized. Epidemics in managed and wildlife populations can lead to considerable economic and biodiversity losses. Yet, we lack understanding of the ecological and evolutionary factors that promote disease emergence. Host-switching viruses may be a particular threat to species important for human welfare, such as pollinating bees. Both honeybees and wild bumblebees have faced sharp declines in the last decades, with high winter mortality seen in honeybees. Infectious and emerging diseases are considered one of the key drivers of declines, acting in synergy with habitat loss and pesticide use. Here I focus on multihost viruses that pose a risk to wild bumblebees. I first identify the risk factors driving viral spillover and emergence from managed honeybees to wild bumblebees, by synthesising current data and literature. Biological factors (i.e. the nature of RNA viruses and ecology of social bees) play a clear role in increasing the risk of disease emergence, but anthropogenic factors (trade and transportation of commercial honeybees and bumblebees) creates the greatest risk of viral spillover to wild bees. Basic knowledge of the pathogenic effect of many common pollinator viruses on hosts other than A. mellifera is currently lacking, yet vital for understanding the wider impacts of infection at a population level. Here, I provide evidence that a common bumblebee virus, Slow bee paralysis virus (SBPV), reduces the longevity of Bombus terrestris under conditions of nutrition stress. The invasion of Varroa destructor as an ectoparasitic viral vector in European honeybees has dramatically altered viral dynamics in honeybees. I test how this specialist honeybee vector affects multi-host pathogens that can infect and be transmitted by both honeybees and wild bumblebees. I sampled across three host species (A. mellifera, B. terrestris and B. pascuorum) from Varroa-free and Varroa-present locations. Using a combination of molecular and phylogenetic techniques I find that this specialist honeybee vector increases the prevalence of four multi-host viruses (deformed wing virus (type A and B), SBPV and black queen cell virus) in sympatric wild bumblebees. Furthermore, wild bumblebees are currently experiencing a DWV epidemic driven by the presence of virus-vectoring Varroa in A. mellifera. Overall this thesis demonstrates that wild bumblebees are at high risk of viral disease emergence. My research adds to the ever-expanding body of evidence indicating that stronger disease controls on commercial bee operations are crucial to protect our wild bumblebees.